Behavioral Ecology Vol. 13 No. 6: 725-727
© 2002 International Society for Behavioral Ecology
Great tits (Parus major) reduce body mass in response to wing area reduction: a field experiment
Museu de Ciencies Naturals (Zoologia), P. Picasso s/n, Parc Ciutadella, 08003 Barcelona, Spain
Address correspondence to J.C. Senar. E-mail: jcsenar{at}mail.bcn.es.
Received 14 November 2000; revised 28 September 2001; accepted 18 December 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Flight performance is crucial in determining whether a small bird will survive an attack by a predator. Given the importance of body mass in determining flight performance, it has been suggested that birds should strategically regulate body mass as a response to predation risk. However, all experiments up to now have been carried out with captive birds, comparing experimental to control birds. Here we present data from the first experiment in the field using a within-individuals experimental design. The wing area of wild great tits, Parus major, was reduced by reversibly taping primaries five to seven. This allowed for the same individual to alternatively act as control or experimental bird. Great tits reduced body mass (but not pectoral muscle width) during episodes of wing area reduction, lending support to the view that the reduction in body mass experienced by birds during molt is a strategy rather than the result of energetic stress. Theoretical models establishing the different trade-offs that determine optimal body mass should therefore take into account this important life-history episode.
Key words: body mass, flight performance, great tits, molt, Parus major, wing area, wing loading.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Flight performance and the ability for fast takeoff is crucial in determining whether a small bird will survive an attack by a predator (Cuthill and Houston, 1997
;
Lima, 1993;
Witter and Cuthill, 1993;
Witter et al., 1994). Wing
loading (body mass/wing area) is a key variable in determining flight
performance (Norberg, 1990;
Pennycuick, 1975;
Rayner, 1990). Because wing
area is more or less fixed within individuals, most research has focused on
how natural variations in body mass (e.g., daily or seasonal fattening) may
determine flight success (Cresswell,
1998; Kullberg,
1998; Kullberg et al.,
1996,
1998;
Lind et al., 1999;
Metcalfe and Ure, 1995;
Van der Veen and Lindström,
2000; Veasey et al.,
1998; Witter et al.,
1994). This is, however, not always the case: natural processes
such as molt or feather abrasion periodically reduce wing area and may
potentially reduce flight performance
(Hedenström and Sunada,
1999; Lind, 2001;
Swaddle et al., 1996,
1999). Thus, it has been
predicted that birds should strategically compensate for the reduction in wing
area by a reduction in body mass (Witter
and Cuthill, 1993). This prediction has been experimentally
confirmed by Swaddle and Witter
(1997) with starlings
Sturnus vulgaris, and by Lind and Jakobsson
(2001) with tree sparrows,
Passer montanus, comparing body mass of birds whose flight feathers
had been cut off at different lengths to that of unmanipulated control birds
(i.e., between-individuals comparison). However, these two studies were
conducted in aviaries, and selection pressures in captivity may differ from
that in the field (e.g., perceived predation risk;
Gentle and Gosler, 2001).
Additionally, as Witter and Cuthill
(1993) have pointed out,
experiments to test for the costs of body mass should ideally be designed to
test for changes in body mass within individuals (i.e., repeated-measures
designs), but such tests are difficult to conduct, especially in the
field. The aim of this study was to provide the first experimental test of body mass regulation using a within-individuals design in the wild. We did this by manipulating the wing area of wild great tits, Parus major, taping several remiges (Figure 1). The advantage of this method in relation to other approaches, such as pulling off or cutting out feathers, is that since the treatment is reversible, it allows the same bird to be used alternatively as experimental individual and control. Using this approach, we demonstrate a causal link between wing area reduction and body mass decrease.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We studied body mass variation in great tits in the suburban area of Barcelona (northeastern Spain) in the summer of 1996. Tits were captured with special peanut-baited funnel traps which allowed the birds to be repeatedly trapped (Senar et al., 1997
).
The traps also worked as permanent feeders, so that highly energetic food
(peanuts) were available to the birds ad libitum during the whole experimental
period. Captures for each experimental unit (see below) were carried out from
dawn to dusk over 2-3 consecutive days. On capture we measured, for each bird,
body mass with an electronic balance (precision 0.1 g), tarsus length with a
digital calliper (precision 0.1 mm), and pectoral muscle width, as measured by
ultrasound (Carrascal et al.,
1998; Newton,
1993). Mass was corrected by regression for body size (tarsus
length) and time of day (hours since dawn) by using the equation, mass = 0.13
+ 0.78 tarsus + 0.12 time (F2,258 = 56.17, p <
.001), which explained 30% of the original variance. Analyses were therefore
carried out on body mass values statistically corrected for tarsus size and
time. Ambient temperature (mean) on the day of capture was not significant
(partial correlation R = -.03, p = .63) and was therefore
not included in the equation. We carried out our experiments during
August—September, at the end of the normal molting period of the species
(Gosler, 1993), to avoid the
interference of unknown seasonal effects. We only used juvenile birds in the
experiments because juveniles do not molt remiges
(Jenni and Winkler, 1994).
Wing area was reduced by taping primary remiges five to seven (counted
ascendantly) (Figure 1). The
taped remiges were separated from the other remiges and positioned such that
their rachises lay side by side. This is the normal spatial relationship of
the three feathers when the wing is folded. A rectangular notch was then cut
from the feather vanes on each side of the rachises along the feather shaft.
Then a strip of tape was attached to the three remiges within the notched
area, around the rachises. Control birds also had the notch cut from the
feather vanes, but no tape was added. Reduction in wing area, measured on a
computer from a digital photograph of an outstretched wing experimentally
taped, was of about 8%, which is within the normal range for birds in molt
(Hedenström, 1998).
Twenty-six birds were trapped during the third week of August (initial capture: 20-21 August); birds were randomly assigned either to the experimental group, which had remiges taped, or to the control group, which was similarly manipulated but with remiges untapped. Two weeks later, birds were retrapped, remeasured (first recapture: 3-4 September) and had treatments reversed, so that control birds had their remiges taped and previous experimental birds had tape removed. Great tits were retrapped and remeasured again during the second week of September (second recapture: 10-12 September). Eighteen birds were captured at the three trapping periods (9 within each treatment). We analyzed body mass variation using repeated-measures ANOVA. Repeated measurements of an individual within a period were averaged. No differences between the two experimental groups of birds were detected in tarsus length (F1,16 = 0.13, p = .72) or trapping hour (F1,182 = 0.61, p = .43).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Average body mass of great tits over the course of the experiment was 16.5 g (SE 0.07, N = 238, including all recaptures). Experimental and control birds did not differ in initial standardized body mass (planned comparison: F1,16 = 0.43, p = .52). However, changes in body mass over the course of the experiment differed according to wing area treatment, indicating that birds alternatively increased or decreased their body mass in response to wing area manipulation (repeated-measures ANOVA, treatment x period interaction: F2,32 = 4.13, p = .03, n = 18 birds; Figure 2). Overall, birds had a lower body mass when their wing area was experimentally reduced than when they were controls (repeated-measures ANOVA comparing experimental vs. control standardized body mass, 16.26 g, SD = 0.82, vs. 16.82 g, SD = 0.70; F1,17 = 11.89, p = .003). Average percentage of variation in body mass was 3.6% (SE = 0.9%; range 0-11.5%; n = 18; comparing second and third experimental periods, see Figure 1). The increase in body mass of control birds during the first 2 weeks of the experiment is probably related to autumn-winter fattening, which is typical for juvenile birds at this time of year (Haftorn, 1976
).
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Pectoral muscle width did not vary over the course of the experiment according to wing-area treatment manipulation (repeated-measures ANOVA, treatment x period interaction: F2,30 = 1.85, p = .17), indicating that variations detected in body mass were not due to variations in muscle width.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Although it has long been clear that fat reserves are insurance against reduced or unpredictable food supplies, it has just now been widely recognized that avian fat storage also entails many different costs mainly associated with predation risk (Cuthill and Houston, 1997
; Witter and Cuthill,
1993). Body mass is therefore considered to reflect the outcome of
this trade-off (Cuthill and Houston,
1997; Houston and McNamara,
1999). Body mass variation according to predation risk
(Carrascal and Polo, 1999;
Gentle and Gosler, 2001;
Gosler et al., 1995;
Lilliendahl, 1997;
Witter et al., 1994) is
thought to operate through the relationship between flight ability and wing
loading (body mass/wing area) and is based on the aerodynamic fact that
increases in body mass may have an important impact on reducing flight
performance (Norberg, 1990;
Witter et al., 1994). However,
empirical results so far obtained are somewhat contradictory, with some
authors finding (Bednekoff,
1996; Kullberg et al.,
1996; Lind, 2001;
Lind et al., 1999;
Metcalfe and Ure, 1995;
Norberg, 1995; Swaddle et al.,
1996,
1999) and some not finding
(Kullberg et al., 1998;
Kullberg, 1998;
Van der Veen and Lindström,
2000; Veasey et al.,
1998) any clear reduction in flight performance because of an
increase in body mass or a reduction in wing area. This disagreement is
probably related, at least in part, to variations in perceived predation risk
by the experimental animals (Carrascal and
Polo, 1999; Veasey et al.,
1998), so that birds performing routine flights probably adjust
their speed to save energy but when under a predator attack sacrifice
energetic considerations for maximum speed
(Veasey et al., 1998).
This interplay of energetic considerations
(Witter and Cuthill, 1993) may
explain why coal tits (Parus ater) reduce body mass when under
predation risk (Carrascal and Polo,
1999), despite the fact that body mass is not critical to flight
performance when escaping from predators
(Kullberg, 1998). Our data on
great tits agrees with this view and clearly shows how birds reduce body mass
as a response to wing area reduction, even though body mass variation may not
be critical in enhancing flight performance when escaping from a predator
(Kullberg et al., 1998).
Hence, the reason for body mass regulation in great tits, as in other species,
may be saving energy (Witter and Cuthill,
1993). This reduction in body mass as an strategic way to
compensate for increased wing loading may be especially important during molt
(Lind and Jakobsson, 2001).
Although our results cannot totally rule out the possibility that changes in
mass are a by-product of changes in foraging efficiency or in the energy cost
of flight (Swaddle and Witter,
1997), the fact that birds were provided with food ad libitum in
feeders highly minimizes its eventual effect. Hence, our results are
consistent with the view that mass may be strategically adjusted to compensate
for changes in wing area. Our study has the enhanced value of having tested
for that relationship within individuals and in the field, where many other
different selective pressures may be simultaneously operating. This gives a
high generality to our results.
It has been suggested that an additional adaptation to reductions in flight
efficiency caused by molt could be an increase in pectoral muscle size, and
this has been found in molting tree sparrows
(Lind and Jakobsson, 2001). We
have not found this relationship in great tits, stressing interspecific
variability in adaptive strategies (Van
der Veen and Lindström, 2000).
Most theoretical frameworks on maintenance of optimal body mass assume that
wing area is more or less fixed within individuals
(Houston and McNamara, 1999).
Given that processes such as molt and feather abrasion periodically reduce
wing area and that at least some bird species adjust their body mass
accordingly (Lind and Jakobsson,
2001; Swaddle and Witter,
1997; this study), models on the strategic regulation of body mass
(Houston and McNamara, 1999)
should take into account this important life-history episode.
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ACKNOWLEDGEMENTS |
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We thank Lluisa Arroyo, Luis María Carrascal, Neil Metcalfe, and Vicente Polo for comments on the manuscript and Hermanitas de la Asunción for permission to work on their properties. L. Arroyo also provided field assistance. This study was supported by D.G.I.C.Y.T. research projects PB92-0044-C02-02 and BOS 2000-0141 of the Spanish Research Council, Ministerio de Educación y Ciencia, and Ministerio de Ciéncia y Tecnología.
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